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First published online December 22, 2008
doi: 10.1242/10.1242/dev.025742
1 Department of Neurology, UCSF School of Medicine, San Francisco, CA 94158,
USA.
2 Cardiovascular Research Institute, UCSF School of Medicine, San Francisco, CA
94158, USA.
3 Department of Medicine, UCSF School of Medicine, San Francisco, CA 94158,
USA.
4 Program in Developmental Biology, UCSF School of Medicine, San Francisco, CA
94158, USA.
5 Program in Neuroscience, UCSF School of Medicine, San Francisco, CA 94158,
USA.
* Authors for correspondence (e-mail: grant.li{at}ucsf.edu; sam.pleasure{at}ucsf.edu)
Accepted 12 November 2008
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SUMMARY |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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Key words: Dentate gyrus, Meninges, Neurogenesis
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INTRODUCTION |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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). There are two well-established regions of adult
neurogenesis in the rodent brain - the subventricular zone (SVZ) and the
dentate gyrus (DG). The SVZ generates new olfactory interneurons involved in
plasticity in the adult olfactory system; and in the DG, new granule neurons
are believed to be involved in learning and memory.
Interestingly, there are stark contrasts in the developmental plan used to
form these two adult neurogenic niches. Many studies have indicated that the
SVZ and the rostral migratory stream are remnants of the embryonic SVZ
(Merkle and Alvarez-Buylla,
2006; Merkle et al.,
2004). By contrast, the DG uses a very distinct developmental plan
to produce a durable neurogenic niche (Li
and Pleasure, 2005). The multi-potential neural precursors seed
the developing dentate gyrus beginning around mid-gestation from their origin
in the medial cortical neuroepithelium. As the scaffolding of the DG forms
around the first postnatal week, the neurogenic precursors settle at the
border between the granule cell layer (GCL) and the hilus, also called the
subgranular zone (SGZ). Migration of multi-potential precursors from one
neurogenic zone (the dentate ventricular zone) to a nascent neurogenic zone
(SGZ) has long been recognized to be a unique reorganization for the cortex,
sharing some features with the migration of granule cell precursors in the
cerebellum.
Previous studies have implicated the Wnt and Shh pathways as regulators of
precursor behavior in the embryonic ventricular zone and SVZ, as well as the
perinatal conversion of the SVZ to its adult state
(Galceran et al., 2000;
Machold et al., 2003;
Pozniak and Pleasure, 2006;
Zhou et al., 2004). In
addition, both of these pathways are involved in the maintenance of precursors
in the postnatal and adult DG (Lai et al.,
2003; Lie et al.,
2005). However, it is not clear what factors regulate the
behaviors of precursors during transit to the DG. In this study, we provide
evidence that en route to the DG, many precursors are localized in a
specialized temporary neurogenic zone before they occupy the nascent DG.
Interestingly, the organization of this zone is controlled by Cajal-Retzius
cell-derived reelin and meningeally produced Cxcl12. By genetic fate-mapping
analysis, we also show that subpial precursors may contribute to the SGZ
formation.
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MATERIALS AND METHODS |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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Immunohistochemistry
Details can be provided on request.
In situ hybridization (ISH)
In situ hybridization protocol and probes (Cxcl12 and Cxcr4) were used as
described (Li et al.,
2008a).
In utero electroporation and DiO Injection
Details can be provided on request.
Glial process tracing
A series of overlapping thin section confocal images were taken with LSM
510 meta two-photon microscope (Carl Zeiss, Inc.). BLBP glial processes were
traced with NIH ImageJ program.
BrdU injection
Timed pregnant mice were intraperitoneally (i.p.) injected with BrdU
(Roche) dissolved in 1xPBS (10 mg/ml) at the dose of 100 mg/kg animal
for acute labeling or 50 mg/kg animal for birthdating analysis.
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).
Quantification
Details can be provided on request.
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RESULTS |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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;
Altman and Bayer, 1990b) showed
that proliferative dentate precursors leave the dentate neuroepithelium and
form a migratory stream into the forming dentate gyrus during late embryonic
development. To better characterize the spatiotemporal dynamics of the
precursors in the dentate migratory stream in mice, we decided to re-examine
this framework with new molecular markers. Using Nestin-GFP transgene and Tbr2
to label the dentate precursors and neurogenic transit amplifying cells,
respectively (Englund et al.,
2005; Yamaguchi et al.,
2000), we revealed the sequential distribution of these cells
during initial dentate gyrus formation. By E14.5, the domain adjacent to the cortical hem in the ventricular zone (VZ) representing the dentate primordium was marked by strong Nestin-GFP expression (Fig. 1A,A1). Concurrently, Tbr2+ cells were abundant in the subventricular zone (SVZ) and a stream of Tbr2+ cells stretched from the SVZ above the forming fimbria to form a line of cells along the pial surface (Fig. 1A2,A4). A day later at E15.5, Nestin-GFP+ cells emanating from the dentate notch formed a narrow stream oriented toward the subpial region at the junction between the fimbria and forming dentate gyrus (Fig. 1B); we have termed this the fimbriodentate junction (FDJ). At high magnification, Tbr2+ cells were also found in the FDJ region (Fig. 1B, B3-4) and, in fact, this structure appeared to have formed as a continuation of the subpial collection of Tbr2+ cells seen at E14.5. Interestingly, in the FDJ, the strongly stained Nestin-GFP+ cells did not overlap with the Tbr2 staining, implying that these were largely non-overlapping cell populations (arrowheads in Fig. 1B1-B4).
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By P2, Nestin-GFP+ cells and processes appeared to spread toward the hilus from the marginal zone (MZ) of the granule cell layer (GCL) (Fig. 1E,E1), but by contrast, most Tbr2+ cells were still restricted to the emerging molecular layer at this stage (Fig. 1E2,E3). At the end of the first postnatal week, most Nestin-GFP+ cells populated the hilus and the subgranular zone (SGZ), and had exited the molecular layer (Fig. 1F,F1). The Tbr2+ population in the molecular layer was reduced and now found largely in the SGZ (arrowhead in Fig. 1F2,F3).
Consistent with work in the adult dentate
(Yamaguchi et al., 2000),
perinatal analysis of Nestin-GFP+ cells with acute BrdU labeling showed that
the subpial Nestin-GFP+ cells close to the HF were actively dividing with
little overlap with Prox1 (see Fig. S1A,A',A'' in the supplementary
material). Similarly, subpial Tbr2+ cells were proliferating (see Fig. S1B in
the supplementary material) with clear distinction from the reelin+
Cajal-Retzius cells (see Fig. S1C in the supplementary material). In agreement
with their neurogenic nature in the developing cortex
(Arnold et al., 2008;
Englund et al., 2005;
Sessa et al., 2008), the weak
Tbr2+ cells also showed low Prox1 expression in both MZ and the newly formed
SGZ at P5 (see Fig. S1D-F in the supplementary material). Taken together, the
spatiotemporal distribution of Nestin-GFP+ and Tbr2+ cells reveal two phases
of neurogenic zone transitions (Fig.
1G1-G4): the dentate VZ-to-subpial transition and the
subpial-to-subgranular transition.
Formation of the transient neurogenic zone coincides with the appearance of transhilar glial processes
Since previous studies indicate that radial glial cells regulate the
morphogenesis of the dentate gyrus
(Eckenhoff and Rakic, 1984;
Rickmann et al., 1987), we
further investigated the distribution of the radial glial scaffolding by GFAP
staining as the Nestin-GFP+ precursors migrate from the dentate primordium to
the subpial neurogenic zone. By E18.5, Prox1+ granule cells already occupied
the forming upper blade, whereas GFAP+ glial fibers were enriched at the
border of the fimbria (Fig.
2A). These GFAP+ fibers appeared to spread out at the entrance of
the hilus and project to the pia all around the forming dentate
(Fig. 2B), whereas Prox1+
granule cells were arranged in parallel to this glial scaffolding in the hilus
(Fig. 2C). Previous studies
assumed that these glial fibers are projecting from radial glial cells with
their cell bodies located in the VZ
(Eckenhoff and Rakic, 1984). To
determine whether these hilar fibers directly project from the dentate VZ or
the new organizing center at the FDJ (Fig.
2B, red arrow), we injected DiO solution into the ventricle of
E18.5 embryos and allowed these to survive for only 3 hours to physically
label all the fibers projecting from the VZ. This labeling prominently marked
all the radial glial fibers spanning the whole hippocampal fields except the
dentate field (Fig. 2D). It
suggests that radial glial fibers in the forming dentate during this migratory
phase do not directly project to the dentate from the dentate ventricular
zone.
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Staining with a radial glial marker, brain lipid binding protein (BLBP), labeled a prominent subset of glial processes in the forming dentate at E18.5 (Fig. 2I). Strikingly, unlike with GFAP staining, glial cell bodies were clearly identifiable with BLBP in the FDJ (arrow in Fig. 2I inset) and some of them had already reached the HF (arrows in Fig. 2J). A collapsed z-projection of the serial sections is shown in Fig. 2J, allowing the reconstruction of two whole BLBP+ cells. The somata of the BLBP+ processes spanning the hilus were pinpointed by tracing the overlapping thin sections (Fig. 2K). Interestingly, somata were found near the FDJ pia or in the hilus (red and yellow arrows in Fig. 2J,K), suggesting that some glia were in the process of migration from the FDJ towards the HF.
Reelin is dispensable for the formation of but controls exit from the transient zone
Numerous studies have shown that reelin secreted from Cajal-Retzius cells
is essential for the development of the neocortex and hippocampus by
controlling the proper lamination of projection neurons
(Rice and Curran, 2001). As
the dentate is also quite abnormal in reelin mutants
(Forster et al., 2002), we
wondered what role reelin plays in the migration of dentate precursors to the
newly identified transient subpial zone. To tackle this issue, we examined the
distribution of Nestin-GFP+ cells at birth in reeler mice. In both the
controls and reeler mice, Nestin-GFP+ or Tbr2+ cells were properly localized
to the subpial zone (arrowheads in Fig.
3A,B and Fig.
3A',B'). Consistent with the known role of reelin in
neuronal migration, Prox1+ granule cells were abnormally distributed across
the dentate field in the mutants (arrow in
Fig. 3D') instead of
forming a relatively compact upper blade as in the controls
(Fig. 3D). Thus, reelin
signaling is required for proper granule cell migration but not for the
subpial localization of Nestin-GFP+ cells.
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2-test, Fig.
3H) in the region outside the marginal zone. Therefore, the
dentate neurogenic niche failed to undergo the subpial-to-subgranular
transition in the absence of functional reelin. Although previous studies
(Forster et al., 2002) suggest
that reelin signaling may cell-autonomously regulate the behavior of radial
glial cells, it is also possible that this role for reelin could be due to a
non-autonomous role for reelin in organizing other cellular components in the
dentate. However, what is clear is that reelin is dispensable for the original
positioning of radial glial and transit-amplifying cells in the subpial zone
but is indispensable for the later reorganization of this zone.
Formation of the subpial zone requires Cxcl12/Cxcr4 signaling
Previous studies indicate that the chemokine Cxcl12 and its cognate
receptor Cxcr4 regulate the morphogenesis of the dentate gyrus
(Bagri et al., 2002;
Lu et al., 2002), but the
mechanistic basis of this defect is not well characterized. More recent
studies suggest the Cxcl12/Cxcr4 signaling plays a crucial role in regulating
the positioning of neurons adjacent to the pia
(Borrell and Marin, 2006;
Li et al., 2008a;
Lopez-Bendito et al., 2008;
Paredes et al., 2006;
Tiveron et al., 2006). Owing
to the expression of Cxcr4 in the migratory stream and subpial zone and
expression of Cxcl12 by the pial meninges (see Fig. S2 in the supplementary
material) (Berger et al.,
2007), we sought to determine whether Cxcl12/Cxcr4 signaling
controls the concentration of Nestin-GFP+ precursors in the subpial region of
the developing dentate. At E18.5 in control animals, Nestin-GFP+ cells
occupied the subpial region around the entire profile of the forming dentate
gyrus from hippocampal fissure superficial to the nascent upper blade and
ventrally to the future lower blade (arrows in
Fig. 4A). In stark contrast, in
Cxcr4-/- mice the Nestin-GFP+ cells were largely scarce in the
subpial region (arrows in Fig.
4B). Consistent with these findings, Tbr2+ cells no longer formed
a compact subpial zone along the FDJ and HF in the Cxcr4 mutants as they did
in controls (white arrows in Fig.
4C,D). Instead, Tbr2+ cells were widely dispersed in the dentate
(yellow arrow in Fig. 4D).
Taken together, these findings indicate that Cxcr4 is required for the proper
formation of the subpial neurogenic zone.
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To determine whether the disruption of the subpial zone and the radial
glial progenitors leads to any dynamic consequences for the cellular output of
the stem/progenitor cells, we analyzed acute BrdU labeling at E18.5. In
agreement with previous studies (Bagri et
al., 2002; Lu et al.,
2002), we found that the number of BrdU+ cells was significantly
decreased in the dentate of Cxcr4 mutants compared with the controls
(Fig. 4I,J). However, this
finding cannot be simply explained by an increase in cell death or a migration
defect resulting from the loss of Cxcr4, as the production of granule cells
did not seem to have drastically declined despite their abnormal distribution
(Fig. 4I,J). We noticed that in
association with the decrease in BrdU+ cell numbers in the Cxcr4 mutants at
E18.5, there was not only an overall decrease in the number of Nestin-GFP+
cells (Fig. 4A,B) but also a
corresponding increase in the number of Tbr2+ cells in the dentate field of
the Cxcr4 mutants compared with the controls
(Fig. 4C,D). This led us to
look into the possibility that dentate precursors prematurely differentiate
into granule cells when they were displaced from the subpial zone. At E15.5, a
robust stream of Nestin-GFP+ cells was present in the controls but it was
diminished in the Cxcr4 mutants (arrows in
Fig. 4K,L). Conversely, the
mutants had a larger patch of Prox1+ granule cells around the FDJ than the
controls. This loss of progenitors and the excess of granule cells at this
early developmental stage suggested the premature differentiation of dentate
progenitors upon displacement from the subpial zone.
To test this more directly, we birthdated granule cells by injecting BrdU at E15.5 and counted the number of BrdU+/Prox1+ cells at E18.5. Interestingly, the density of double-labeled cells was dramatically higher in the mutants (227±21%) compared with controls (n=4, *P<0.05, Student's t-test). However, when BrdU was administered at E16.5, the density of BrdU+/Prox1+ cells was significantly lower in mutants Cxcr4 mutants (51.7±7.5%) than controls (n=4, *P<0.01, Student's t-test) (Fig. 4O). This indicates that mutant mice have an early excessive burst of production of granule neurons but fail to produce the appropriate number of granule cells only a day later. Taken together, these data indicate that progenitors displaced from the subpial zone prematurely differentiate and the localization to the subpial transient zone may be required to maintain dentate precursors in an undifferentiated state during late embryonic stages.
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)
(Emx1-Cxcr4 cKO thereafter) to bypass the prenatal lethality of null Cxcr4.
The prenatal development of the dentate gyrus in Emx1-Cxcr4 cKO resembled the
null mutants with Tbr2 and Prox1 staining (see Fig. S3 in the supplementary
material). By P5, there was distinct reorganization of the radial glial scaffolding in control mice shown by the Nestin-GFP+ cells at the SGZ, whereas in the cKO mice the Nestin-GFP+ cells were scattered throughout the dentate formation (see Fig. S4A,B in the supplementary material). However, the distribution patterns of Tbr2+ or Ki67+ cells showed subtle differences between controls and cKOs (see Fig. S4C-F in the supplementary material). Surprisingly, despite the prenatal abnormalities in the early GCL of the Cxcr4-/- and the Emx1-Cxcr4 cKO, Prox1+ cells formed distinct upper and lower blades of GCLs in the cKO mice (see Fig. S4G,H in the supplementary material). Our data suggests the granule cells are largely able to adopt appropriate layer positioning in Emx1-Cxcr4 cKO despite the early defects in SPZ.
At P14, Emx1-Cxcr4 cKOs showed almost normal organization of the SGZ with BLBP, Tbr2 and BrdU (see Fig. S4I-N in the supplementary material) and GCL with Prox1 (see Fig. S4O-P in the supplementary material). This recovery was sustained into adulthood (see Fig. S5 in the supplementary material). As the cre activity of Emx1ires-cre completely covered dentate primordium at E14.5 and showed complete recombination at P14 (see Fig. S6A-F in the supplementary material), low penetrance of Emx1ires-cre is unlikely to explain the developmental recovery in the cKO mice.
One possible explanation for the SGZ recovery in the Emx1-Cxcr4 cKOs is
that other ligand-receptor systems may compensate for the loss of Cxcr4. To
test this, pertussis toxin (PTX) expression
(Regard et al., 2007) was
conditionally activated by Emx1ires-cre (Emx1-PTX thereafter),
potently blocking all the trimeric Gi/o signaling including Cxcr4.
As expected, the perinatal subpial neurogenic zone did not properly form in
the Emx1-PTX animals (see Fig. S7 in the supplementary material). By P4,
Nestin-GFP+ cells were distributed as patches scattered throughout the dentate
(Fig. 5A,B) and both Ki67+ and
Tbr2+ cells were chaotically dispersed throughout the whole dentate
(Fig. 5C-F). Prox1+ granule
cells also failed to assume their distinct layered organization and many were
ectopically located in the subpial region of FDJ
(Fig. 5G,H). Emx1-PTX animals
died in the second postnatal week, so we chose P10 animals for further
analysis. Compared with the controls (Fig.
5I,K,M,O), Emx1-PTX animals almost complete lost organization of
the BLBP+ scaffolding in the SGZ (Fig.
5J); furthermore, Tbr2+ neurogenic precursors and the BrdU+ or
Ki67+ cycling cells in the SGZ were also ectopically localized in the MZ, GCL
and hilus (Fig. 5L,N,P). In
addition, the border between the hilus and Prox1+ GCL was obscured owing to
ectopic dispersion of granule cells into the hilus and granule cell
heterotopias were visible in the remnant of the migratory stream to the
dentate (Fig. 5Q,R). Therefore,
the formation of SGZ appears to rely on a PTX-sensitive pathway.
Contribution of subpial progenitors to the formation of the subgranular zone
Previous genetic fate-mapping analysis with the Gli1CreERT2 line
revealed that the self-renewing stem cells in the dentate gyrus first appear
at the late embryogenesis (Ahn and Joyner,
2005). In order to test whether the SPZ progenitors may contribute
to the neural stem cells settled in the SGZ, we reasoned that when tamoxifen
(TM) was injected at E17.5 into the Gli1CreERT2 line in the
presence of Rosa-lacZ reporter, the labeled cells would initially
emerge from the subpial zone and then spread toward the GCL from there over
time. If the hilar progenitors exclusively contribute to the SGZ, we would
expect the opposite. Interestingly, after 24 hours, lacZ+ cells were
first detected in the MZ (inset 1 in Fig.
6A) and the edge between MZ and GCL (inset 2 in
Fig. 6A) in the upper blade.
After 48 hours, lacZ+ spread across the GCL and SGZ in the upper
blade (Fig. 6B and inset). When
tamoxifen was administered at E18.5 and lacZ expression was analyzed
24 hours later, we found most lacZ+ cells were restricted in the GCL
of the upper blade (Fig. 6C and
inset) and others were observed in the future lower blade
(Fig. 6C). To further analyze
the cellular identity of cells produced after recombination induced at E17.5,
we turned to the RosaYFP reporter line. The earliest GFP+ cells were detected
at P0 (Fig. 6D) and did not
express Prox1 (Fig. 6E). In
other cases, it appeared that a cell might have just divided and Prox1 could
be detected in one of the GFP+ doublet cells (arrows in
Fig. 6F,F'). When cell
fates were mapped in animals at P14, most recombined cells were Prox1+ granule
cells (Fig. 6G, inset), and a
few of them showed radial glial morphology
(Fig. 6H,I) and were co-labeled
with BLBP (Fig. 6H,H') or
GFAP (Fig. 6I,I'). Taken
together, these findings support the idea that perinatal subpial progenitors
contribute to the neural stem cells that eventually settle in the SGZ.
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DISCUSSION |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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A novel, temporary neurogenic zone in the developing dentate gyrus adjacent to the meninges
The most distinct feature of dentate development compared with other
forebrain areas is the extended migration of neural precursors from the VZ to
a newly formed region in the SGZ. The SGZ is a long-lived durable niche that
allows survival and self-renewal of neural stem cells. But how do neural
precursors manage to traverse the territories from VZ to ultimately form SGZ?
This is not a small hurdle, because at the stage that precursors begin to exit
the VZ there is no formed dentate gyrus or SGZ for them to occupy.
Our analysis of the Nestin-GFP transgene in combination with transit
amplifying cell marker Tbr2 shows that neurogenic precursors initially follow
a subpial migratory route to fimbriodentate junction, some then move across
the hilus and take residence in the subpial region of the hippocampal fissure
leaving a population of progenitors adjacent to the pia around the entire pole
of the dentate (Fig. 7). From
this base of operations, neurogenic precursors generate Tbr2+ transient
amplifying cells and then granule neurons that form the initial structure of
the dentate granule cell layer. Nestin-GFP+ and Tbr2+ cells gradually
disappear from the subpial region in the first postnatal week, both cell types
accordingly increase in the SGZ and hilus, suggesting there is a
subpial-to-hilar transition. In agreement with our findings, Ngn2 mutant mice
were recently shown to have severe neurogenic defects in the developing
dentate gyrus and using a Ngn2-GFP mouse line the same authors found a similar
group of neurogenic precursors was in close proximity to the subpial zone
(Galichet et al., 2008).
Complex organization of the transient neurogenic zone in the developing dentate gyrus
The transient subpial zone is regulated by Cxcl12 secreted from meningeal
fibroblasts and reelin from the Cajal-Retzius cells in the dentate marginal
zone. It is interesting to consider what other factors may be important in the
constitution of this zone and their ability to maintain dentate progenitors in
an undifferentiated state (Fig.
7B). The analysis of the mutants in the canonical Wnt signaling
pathway suggests that Wnts play a crucial role in the expansion and
maintenance of the dentate precursor pool during this same developmental
period (Galceran et al., 2000;
Grove et al., 1998;
Lee et al., 2000;
Zhou et al., 2004). Also shown
to be active and required for the formation of dentate stem cell niches is
sonic hedgehog (Shh) (Machold et al.,
2003). However, it is not clear which cells express Shh or Wnts in
the subpial zone. There is evidence that the subgranular zone niche is
intimately associated with blood vessels
(Palmer et al., 2000) and that
endothelial cells may provide important regulators to stem cell behaviors
(Shen et al., 2004). These
findings may have relevance to the timing and importance of the subpial
zone.
The roles of Gi/o signaling pathway in stem cell migration and maintenance
The loss of Cxcr4 only transiently affects the formation of the SGZ despite
the disorganization of the transient SPZ. Prominent roles for other chemokines
and their receptors have been postulated in the dentate gyrus
(Tran et al., 2007). The
redundancy of signaling pathways is evidenced by our use of the recently
developed Cre-mediated PTX expression line
(Regard et al., 2007). These
mice have a very dramatic developmental dentate phenotype, which suggests the
search for other Gi/o-coupled receptor/ligand combinations in the
dentate gyrus is likely to result in both other important developmental
regulators of dentate morphogenesis but also perhaps potent molecular targets
to design reagents to regulate dentate neurogenesis.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/136/2/327/DC1
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Footnotes |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
|---|
Ahn, S. and Joyner, A. L. (2005). In vivo
analysis of quiescent adult neural stem cells responding to Sonic hedgehog.
Nature 437,894
-897.[CrossRef][Medline]
Altman, J. and Bayer, S. A. (1990a). Migration
and distribution of two populations of hippocampal granule cell precursors
during the perinatal and postnatal periods. J. Comp.
Neurol. 301,365
-381.[CrossRef][Medline]
Altman, J. and Bayer, S. A. (1990b). Mosaic
organization of the hippocampal neuroepithelium and the multiple germinal
sources of dentate granule cells. J. Comp. Neurol.
301,325
-342.[CrossRef][Medline]
Arnold, S. J., Huang, G. J., Cheung, A. F., Era, T., Nishikawa,
S., Bikoff, E. K., Molnar, Z., Robertson, E. J. and Groszer, M.
(2008). The T-box transcription factor Eomes/Tbr2 regulates
neurogenesis in the cortical subventricular zone. Genes
Dev. 22,2479
-2484.
Bagri, A., Gurney, T., He, X., Zou, Y. R., Littman, D. R.,
Tessier-Lavigne, M. and Pleasure, S. J. (2002). The chemokine
SDF1 regulates migration of dentate granule cells.
Development 129,4249
-4260.[Medline]
Berger, O., Li, G., Han, S. M., Paredes, M. and Pleasure, S.
J. (2007). Expression of SDF-1 and CXCR4 during
reorganization of the postnatal dentate gyrus. Dev.
Neurosci. 29,48
-58.[CrossRef][Medline]
Borrell, V. and Marin, O. (2006). Meninges
control tangential migration of hem-derived Cajal-Retzius cells via
CXCL12/CXCR4 signaling. Nat. Neurosci.
9,1284
-1293.[CrossRef][Medline]
Eckenhoff, M. F. and Rakic, P. (1984). Radial
organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and
immunocytochemical analysis in the developing rhesus monkey. J.
Comp. Neurol. 223,1
-21.[CrossRef][Medline]
Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A., Bulfone,
A., Kowalczyk, T. and Hevner, R. F. (2005). Pax6, Tbr2, and
Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells,
and postmitotic neurons in developing neocortex. J.
Neurosci. 25,247
-251.
Forster, E., Tielsch, A., Saum, B., Weiss, K. H., Johanssen, C.,
Graus-Porta, D., Muller, U. and Frotscher, M. (2002). Reelin,
Disabled 1, and beta 1 integrins are required for the formation of the radial
glial scaffold in the hippocampus. Proc. Natl. Acad. Sci.
USA 99,13178
-13183.
Gage, F. H. (2000). Mammalian neural stem
cells. Science 287,1433
-1438.
Galceran, J., Miyashita-Lin, E. M., Devaney, E., Rubenstein, J.
L. and Grosschedl, R. (2000). Hippocampus development and
generation of dentate gyrus granule cells is regulated by LEF1.
Development 127,469
-482.[Abstract]
Galichet, C., Guillemot, F. and Parras, C. M.
(2008). Neurogenin 2 has an essential role in development of the
dentate gyrus. Development
135,2031
-2041.
Gorski, J. A., Talley, T., Qiu, M., Puelles, L., Rubenstein, J.
L. and Jones, K. R. (2002). Cortical excitatory neurons and
glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage.
J. Neurosci. 22,6309
-6314.
Grove, E. A., Tole, S., Limon, J., Yip, L. and Ragsdale, C.
W. (1998). The hem of the embryonic cerebral cortex is
defined by the expression of multiple Wnt genes and is compromised in
Gli3-deficient mice. Development
125,2315
-2325.[Abstract]
Lai, K., Kaspar, B. K., Gage, F. H. and Schaffer, D. V.
(2003). Sonic hedgehog regulates adult neural progenitor
proliferation in vitro and in vivo. Nature Neurosci.
6, 21-27.[CrossRef][Medline]
Lee, S. M., Tole, S., Grove, E. and McMahon, A. P.
(2000). A local Wnt-3a signal is required for development of the
mammalian hippocampus. Development
127,457
-467.[Abstract]
Li, G. and Pleasure, S. J. (2005).
Morphogenesis of the dentate gyrus: what we are learning from mouse mutants.
Dev. Neurosci. 27,93
-99.[CrossRef][Medline]
Li, G., Adesnik, H., Li, J., Long, J., Nicoll, R. A.,
Rubenstein, J. L. R. and Pleasure, S. J. (2008a). Regional
distribution of cortical interneurons and development of inhibitory tone are
regulated by Cxcl12/Cxcr4 signaling. J. Neurosci
28,1085
-1098.
Li, G., Berger, O., Han, S. M., Paredes, M., Wu, N. C. and
Pleasure, S. J. (2008b). Hilar mossy cells share
developmental influences with dentate granule neurons. Dev.
Neurosci. 30,255
-261.[CrossRef][Medline]
Lie, D. C., Colamarino, S. A., Song, H. J., Desire, L., Mira,
H., Consiglio, A., Lein, E. S., Jessberger, S., Lansford, H., Dearie, A. R. et
al. (2005). Wnt signalling regulates adult hippocampal
neurogenesis. Nature
437,1370
-1375.[CrossRef][Medline]
Lopez-Bendito, G., Sanchez-Alcaniz, J. A., Pla, R., Borrell, V.,
Pico, E., Valdeolmillos, M. and Marin, O. (2008). Chemokine
signaling controls intracortical migration and final distribution of GABAergic
interneurons. J. Neurosci.
28,1613
-1624.
Lu, M., Grove, E. A. and Miller, R. J. (2002).
Abnormal development of the hippocampal dentate gyrus in mice lacking the
CXCR4 chemokine receptor. Proc. Natl. Acad. Sci. USA
99,7090
-7095.
Machold, R., Hayashi, S., Rutlin, M., Muzumdar, M. D., Nery, S.,
Corbin, J. G., Gritli-Linde, A., Dellovade, T., Porter, J. A., Rubin, L. L. et
al. (2003). Sonic hedgehog is required for progenitor cell
maintenance in telencephalic stem cell niches. Neuron
39,937
-950.[CrossRef][Medline]
Merkle, F. T. and Alvarez-Buylla, A. (2006).
Neural stem cells in mammalian development. Curr. Opin. Cell
Biol. 18,704
-709.[CrossRef][Medline]
Merkle, F. T., Tramontin, A. D., Garcia-Verdugo, J. M. and
Alvarez-Buylla, A. (2004). Radial glia give rise to adult
neural stem cells in the subventricular zone. Proc. Natl. Acad.
Sci. USA 101,17528
-17532.
Palmer, T. D., Willhoite, A. R. and Gage, F. H.
(2000). Vascular niche for adult hippocampal neurogenesis.
J. Comp. Neurol. 425,479
-494.[CrossRef][Medline]
Paredes, M. F., Li, G., Berger, O., Baraban, S. C. and Pleasure,
S. J. (2006). Stromal-derived factor-1 (CXCL12) regulates
laminar position of Cajal-Retzius cells in normal and dysplastic brains.
J. Neurosci. 26,9404
-9412.
Pozniak, C. D. and Pleasure, S. J. (2006). A
tale of two signals: Wnt and Hedgehog in dentate neurogenesis. Sci
STKE 2006, pe5.
Regard, J. B., Kataoka, H., Cano, D. A., Camerer, E., Yin, L.,
Zheng, Y. W., Scanlan, T. S., Hebrok, M. and Coughlin, S. R.
(2007). Probing cell type-specific functions of G(i) in vivo
identifies GPCR regulators of insulin secretion. J. Clin.
Invest. 117,4034
-4043.[CrossRef][Medline]
Rice, D. S. and Curran, T. (2001). Role of the
reelin signaling pathway in central nervous system development.
Annu. Rev. Neurosci. 24,1005
-1039.[CrossRef][Medline]
Rickmann, M., Amaral, D. G. and Cowan, W. M.
(1987). Organization of radial glial cells during the development
of the rat dentate gyrus. J. Comp. Neurol.
264,449
-479.[CrossRef][Medline]
Sessa, A., Mao, C. A., Hadjantonakis, A. K., Klein, W. H. and
Broccoli, V. (2008). Tbr2 directs conversion of radial glia
into basal precursors and guides neuronal amplification by indirect
neurogenesis in the developing neocortex. Neuron
60, 56-69.[CrossRef][Medline]
Shen, Q., Goderie, S. K., Jin, L., Karanth, N., Sun, Y.,
Abramova, N., Vincent, P., Pumiglia, K. and Temple, S.
(2004). Endothelial cells stimulate self-renewal and expand
neurogenesis of neural stem cells. Science
304,1338
-1340.
Tiveron, M. C., Rossel, M., Moepps, B., Zhang, Y. L.,
Seidenfaden, R., Favor, J., Konig, N. and Cremer, H. (2006).
Molecular interaction between projection neuron precursors and invading
interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the
cortical subventricular zone/intermediate zone. J.
Neurosci. 26,13273
-13278.
Tran, P. B., Banisadr, G., Ren, D. J., Chenn, A. and Miller, R.
J. (2007). Chemokine receptor expression by neural progenitor
cells in neurogenic regions of mouse brain. J. Comp.
Neurol. 500,1007
-1033.[CrossRef][Medline]
Yamaguchi, M., Saito, H., Suzuki, M. and Mori, K.
(2000). Visualization of neurogenesis in the central nervous
system using nestin promoter-GFP transgenic mice.
NeuroReport 11,1991
-1996.[Medline]
Zhou, C. J., Zhao, C. and Pleasure, S. J.
(2004). Wnt signaling mutants have decreased dentate granule cell
production and radial glial scaffolding abnormalities. J.
Neurosci. 24,121
-126.
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